Ttc30a affects tubulin modifications in a model for ciliary chondrodysplasia with polycystic kidney disease

Proc Natl Acad Sci U S A. 2021 Sep 28;118(39):e2106770118. doi: 10.1073/pnas.2106770118.

Abstract

Skeletal ciliopathies (e.g., Jeune syndrome, short rib polydactyly syndrome, and Sensenbrenner syndrome) are frequently associated with nephronophthisis-like cystic kidney disease and other organ manifestations. Despite recent progress in genetic mapping of causative loci, a common molecular mechanism of cartilage defects and cystic kidneys has remained elusive. Targeting two ciliary chondrodysplasia loci (ift80 and ift172) by CRISPR/Cas9 mutagenesis, we established models for skeletal ciliopathies in Xenopus tropicalis Froglets exhibited severe limb deformities, polydactyly, and cystic kidneys, closely matching the phenotype of affected patients. A data mining-based in silico screen found ttc30a to be related to known skeletal ciliopathy genes. CRISPR/Cas9 targeting replicated limb malformations and renal cysts identical to the models of established disease genes. Loss of Ttc30a impaired embryonic renal excretion and ciliogenesis because of altered posttranslational tubulin acetylation, glycylation, and defective axoneme compartmentalization. Ttc30a/b transcripts are enriched in chondrocytes and osteocytes of single-cell RNA-sequenced embryonic mouse limbs. We identify TTC30A/B as an essential node in the network of ciliary chondrodysplasia and nephronophthisis-like disease proteins and suggest that tubulin modifications and cilia segmentation contribute to skeletal and renal ciliopathy manifestations of ciliopathies in a cell type-specific manner. These findings have implications for potential therapeutic strategies.

Keywords: Xenopus; chondrodysplasia; cilia; cystic kidney disease; tubulin modifications.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone and Bones / abnormalities*
  • Bone and Bones / metabolism
  • Bone and Bones / pathology
  • Ciliopathies / genetics
  • Ciliopathies / metabolism
  • Ciliopathies / pathology*
  • Craniosynostoses / genetics
  • Craniosynostoses / metabolism
  • Craniosynostoses / pathology*
  • Cytoskeletal Proteins / genetics
  • Cytoskeletal Proteins / metabolism*
  • Disease Models, Animal
  • Ectodermal Dysplasia / genetics
  • Ectodermal Dysplasia / metabolism
  • Ectodermal Dysplasia / pathology*
  • Embryo, Nonmammalian / metabolism
  • Embryo, Nonmammalian / pathology*
  • Musculoskeletal Abnormalities / genetics
  • Musculoskeletal Abnormalities / metabolism
  • Musculoskeletal Abnormalities / pathology*
  • Phenotype
  • Polycystic Kidney Diseases / genetics
  • Polycystic Kidney Diseases / metabolism
  • Polycystic Kidney Diseases / pathology*
  • Tubulin / chemistry*
  • Tubulin / metabolism
  • Xenopus laevis

Substances

  • Cytoskeletal Proteins
  • Tubulin

Supplementary concepts

  • Cranioectodermal Dysplasia